Transition from metal-DTH resistance to susceptibility is facilitated by NLRP3 inflammasome signaling induced Th17 reactivity: Implications for orthopedic implants

PLoS One. 2019 Jan 17;14(1):e0210336. doi: 10.1371/journal.pone.0210336. eCollection 2019.

Abstract

Metal hypersensitivity has been recognized as an adverse biologic reaction that can compromise total joint arthroplasty (TJA) performance. However, the etiology of metal hypersensitivity responses in TJAs remains unclear. Metal implant debris is known to act as a danger signal that drives NLRP3 inflammasome activation. It remains unknown if implant debris induced inflammasome activation regulates T cell lineage in TJA metal hypersensitivity responses. In this study, we show both in vivo and in vitro that the pathogenesis of metal hypersensitivity responses to implant debris are largely dependent on activation of the inflammasome/caspase-1 pathway and subsequent production of IL-17A/F by CD4+ T cells. Inhibiting either the inflammasome pathway or IL-17A bioactivity in vivo and in vitro (in vivo using NLRP3 and Caspase-1 deficient mice or in vitro using blocking agents such as Capase-1 inhibitor, IL-1Ra and anti-IL-17A), significantly (p<0.05) mitigated metal-DTH paw inflammation as well as lymphocyte cytokine (IFN-γ and IL-17) and proliferation responses in metal-sensitized mice and primary human PBMCs. This study provides mechanistic insight into how in vivo exposure to orthopedic implant debris, and metals in general, elicits NLRP3 inflammasome activation that mediates the generation of IL-17A/F producing CD4+ T cells, leading to metal-delayed type hypersensitivity reactions.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Caspase 1 / deficiency
  • Caspase 1 / genetics
  • Caspase 1 / immunology
  • Cells, Cultured
  • Cytokines / biosynthesis
  • Female
  • Humans
  • Hypersensitivity, Delayed / etiology*
  • Hypersensitivity, Delayed / immunology
  • In Vitro Techniques
  • Inflammasomes / immunology*
  • Interleukin-17 / antagonists & inhibitors
  • Interleukin-17 / immunology
  • Joint Prosthesis / adverse effects*
  • Metals / adverse effects*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Immunological
  • NLR Family, Pyrin Domain-Containing 3 Protein / deficiency
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / immunology*
  • Nickel / adverse effects
  • Prosthesis Failure / etiology
  • Signal Transduction
  • Th17 Cells / immunology*

Substances

  • Cytokines
  • Inflammasomes
  • Interleukin-17
  • Metals
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Nickel
  • Casp1 protein, mouse
  • Caspase 1